Diversity of KaiC-based timing systems in marine Cyanobacteria

Marine Genomics

Volumn 14, Issue , 2014, Pages 3-16

  Axmann, Ilka M ^a,d   Hertel, Stefanie ^a   Wiegard, Anika ^a   Dörrich, Anja K ^b   Wilde, Annegret ^c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Circadian clock; Diversity; KaiC; Marine Cyanobacteria

Indexed keywords

CYANOBACTERIA; EUKARYOTA; KAIA; PROCHLOROCOCCUS; PROCHLOROCOCCUS MARINUS; PROKARYOTA; SYNECHOCOCCUS ELONGATUS; SYNECHOCOCCUS ELONGATUS PCC 6301; SYNECHOCOCCUS ELONGATUS PCC 7942;

BACTERIAL PROTEIN; CIRCADIAN RHYTHM SIGNALING PROTEIN; KAIC PROTEIN, CYANOBACTERIA;

AMINO ACID SEQUENCE; CIRCADIAN RHYTHM; CYANOBACTERIUM; GENETIC VARIABILITY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CIRCADIAN RHYTHM SIGNALING PEPTIDES AND PROTEINS; CYANOBACTERIA; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84902834100     PISSN: 18747787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.margen.2013.12.006     Document Type: Review

References (166)

1. Akiyama S., Nohara A., Ito K., Maéda Y. Assembly and disassembly dynamics of the cyanobacterial periodosome. Mol. Cell 2008, 29:703-716.
2. Aoki S., Onai K. Circadian clocks of Synechocystis sp. strain PCC 6803, Thermosynechococcus elongatus, Prochlorococcus spp., Trichodesmium spp. and other species. Bacterial Circadian Programs 2009, 259-282. Springer, Berlin Heidelberg. J.L. Ditty, S.R. Mackey, C.H. Johnson (Eds.).
3. Arita K., Hashimoto H., Igari K., Akaboshi M., Kutsuna S., Sato M., Shimizu T. Structural and biochemical characterization of a cyanobacterium circadian clock-modifier protein. J. Biol. Chem. 2007, 282:1128-1135.
4. Axmann I.M., Dühring U., Seeliger L., Arnold A., Vanselow J.T., Kramer A., Wilde A. Biochemical evidence for a timing mechanism in Prochlorococcus. J. Bacteriol. 2009, 191:5342-5347.
5. Baca I., Sprockett D., Dvornyk V. Circadian input kinases and their homologs in Cyanobacteria: evolutionary constraints versus architectural diversification. J. Mol. Evol. 2010, 70:453-465.
6. Beard S.J., Hayes P.K., Pfeifer F., Walsby A.E. The sequence of the major gas vesicle protein, GvpA, influences the width and strength of halobacterial gas vesicles. FEMS Microbiol. Lett. 2002, 213:149-157.
7. Bell-Pedersen D., Cassone V.M., Earnest D.J., Golden S.S., Hardin P.E., Thomas T.L., Zoran M.J. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 2005, 6:544-556.
8. Berman-Frank I., Lundgren P., Chen Y.B., Kupper H., Kolber Z., Bergman B., Falkowski P. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 2001, 294:1534-1537.
9. Bothe H., Tripp H.J., Zehr J.P. Unicellular Cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed. Arch. Microbiol. 2010, 192:783-790.
10. Bourne H.R., Sanders D.A., McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature 1991, 349:117-127.
11. Brettschneider C., Rose R.J., Hertel S., Axmann I.M., Heck A.J., Kollmann M. A sequestration feedback determines dynamics and temperature entrainment of the KaiABC circadian clock. Mol. Syst. Biol. 2010, 6:389.
12. Bruyant F., Babin M., Sciandra A., Marie D., Genty B., Claustre H., Blanchot J., Bricaud A., Rippka R., Boulben S., Louis F., Partensky F. An axenic cyclostat of Prochlorococcus PCC 9511 with a simulator of natural light regimes. J. Appl. Phycol. 2001, 13:135-142.
13. Bruyant F., Babin M. Diel variations in the photosynthetic parameters of Prochlorococcus strain PCC 9511: combined effects of light and cell cycle. Limnol. Oceanogr. 2005, 50:850-863.
14. Bryant D.A. The beauty in small things revealed. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9647-9649.
15. Cerveny J., Sinetova M.A., Valledor L., Sherman L.A., Nedbal L. Ultradian metabolic rhythm in the diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:13210-13215.
16. Chang Y.G., Tseng R., Kuo N.W., LiWang A. Rhythmic ring-ring stacking drives the circadian oscillator clockwise. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:16847-16851.
17. Chen Y., Kim Y.-I., Mackey S.R., Holtman C.K., LiWang A., Golden S.S. A novel allele of kaiA shortens the circadian period and strengthens interaction of oscillator components in the cyanobacterium Synechococcus elongatus PCC 7942. J. Bacteriol. 2009, 191:4392-4400.
18. Chen Y.B., Zehr J.P., Mellon M. Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. Ims 101 in defined media: evidence for a circadian rhythm. J. Phycol. 1996, 32:916-923.
19. Chen Y.B., Dominic B., Zani S., Mellon M.T., Zehr J.P. Expression of photosynthesis genes in relation to nitrogen fixation in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101. Plant Mol. Biol. 1999, 41:89-104.
20. Church M.J., Jenkins B.D., Karl D.M., Zehr J.P. Vertical distributions of nitrogen-fixing phylotypes at Stn Aloha in the oligotrophic North Pacific Ocean. Aquat. Microb. Ecol. 2005, 38:3-14.
21. Claustre H., Bricaud A., Babin M., Bruyant F., Guillou L., Le Gall F., Marie D., Partensky F. Diel variations in Prochlorococcus optical properties. Limnol. Oceanogr. 2002, 47:1637-1647.
22. Clodong S., Dühring U., Kronk L., Wilde A., Axmann I., Herzel H., Kollmann M. Functioning and robustness of a bacterial circadian clock. Mol. Syst. Biol. 2007, 3:90.
23. Damerval T., Castets A.M., Guglielmi G., Houmard J., Tandeau de Marsac N. Occurrence and distribution of gas vesicle genes among Cyanobacteria. J. Bacteriol. 1989, 171:1445-1452.
24. Damerval T., Castets A.M., Houmard J., Tandeau de Marsac N. Gas vesicle synthesis in the cyanobacterium Pseudanabaena sp.: occurrence of a single photoregulated gene. Mol. Microbiol. 1991, 5:657-664.
25. Damiola F., Le Minh N., Preitner N., Kornmann B., Fleury-Olela F., Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000, 14:2950-2961.
26. Dong G., Yang Q., Wang Q., Kim Y.I., Wood T.L., Osteryoung K.W., van Oudenaarden A., Golden S.S. Elevated ATPase activity of KaiC applies a circadian checkpoint on cell division in Synechococcus elongatus. Cell 2010, 140:529-539.
27. Dvornyk V., Vinogradova O., Nevo E. Origin and evolution of circadian clock genes in prokaryotes. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2495-2500.
28. Dvornyk V., Deng H.W., Nevo E. Structure and molecular phylogeny of sasA genes in Cyanobacteria: insights into evolution of the prokaryotic circadian system. Mol. Biol. Evol. 2004, 21:1468-1476.
29. Edgar R.S., Green E.W., Zhao Y., van Ooijen G., Olmedo M., Qin X., Xu Y., Pan M., Valekunja U.K., Feeney K.A., Maywood E.S., Hastings M.H., Baliga N.S., Merrow M., Millar A.J., Johnson C.H., Kyriacou C.P., O'Neill J.S., Reddy A.B. Peroxiredoxins are conserved markers of circadian rhythms. Nature 2012, 485:459-464.
30. Egli M., Mori T., Pattanayek R., Xu Y., Qin X., Johnson C.H. Dephosphorylation of the core clock protein KaiC in the cyanobacterial KaiABC circadian oscillator proceeds via an ATP synthase mechanism. Biochemistry 2012, 51:1547-1558.
31. Egli M., Pattanayek R., Sheehan J.H., Xu Y., Mori T., Smith J.A., Johnson C.H. Loop-loop interactions regulate KaiA-stimulated KaiC phosphorylation in the cyanobacterial KaiABC circadian clock. Biochemistry 2013, 52:1208-1220.
32. Egli M., Johnson C.H. A circadian clock nanomachine that runs without transcription or translation. Curr. Opin. Neurobiol. 2013, 23:1-9.
33. Emery P., So W.V., Kaneko M., Hall J.C., Rosbash M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 1998, 95:669-679.
34. Fay P., Stewart W.D., Walsby A.E., Fogg G.E. Is the heterocyst the site of nitrogen fixation in blue-green algae?. Nature 1968, 220:810-812.
35. Fay P. Heterocyst isolation. Methods Enzymol. 1980, 69:801-812.
36. Gallon J.R., LaRue T.A., Kurz W.G. Photosynthesis and nitrogenase activity in the blue-green alga Gloeocapsa. Can. J. Microbiol. 1974, 20:1633-1637.
37. Garczarek L., Partensky F., Irlbacher H., Holtzendorff J., Babin M., Mary I., Thomas J.C., Hess W.R. Differential expression of antenna and core genes in Prochlorococcus PCC 9511 (Oxyphotobacteria) grown under a modulated light-dark cycle. Environ. Microbiol. 2001, 3:168-175.
38. Goericke R., Welschmeyer N.A. The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep-Sea Res. 1993, 40:2283-2294.
39. Golden S.S., Brusslan J., Haselkorn R. Genetic engineering of the cyanobacterial chromosome. Methods Enzymol. 1987, 153:215-231.
40. Golden S.S. Mutagenesis of Cyanobacteria by classical and gene-transfer-based methods. Methods Enzymol. 1988, 167:714-727.
41. Gonze D., Roussel M.R., Goldbeter A. A model for the enhancement of fitness in Cyanobacteria based on resonance of a circadian oscillator with the external light-dark cycle. J. Theor. Biol. 2002, 214:577-597.
42. Green J.W., Knoll A.H., Swett K. Microfossils from silicified stromatolitic carbonates of the Upper Proterozoic Limestone-Dolomite 'Series', central East Greenland. Geol. Mag. 1989, 126:567-585.
43. Gutu A., O'Shea E.K. Two antagonistic clock-regulated histidine kinases time the activation of circadian gene expression. Mol. Cell 2013, 50:288-294.
44. Hanaoka M., Takai N., Hosokawa N., Fujiwara M., Akimoto Y., Kobori N., Iwasaki H., Kondo T., Tanaka K. RpaB, another response regulator operating circadian clock-dependent transcriptional regulation in Synechococcus elongatus PCC 7942. J. Biol. Chem. 2012, 287:26321-26327.
45. Haselkorn R. Heterocysts. Annu. Rev. Plant Physiol. 1978, 29:319-344.
46. Hayashi F., Suzuki H., Iwase R., Uzumaki T., Miyake A., Shen J.R., Imada K., Furukawa Y., Yonekura K., Namba K., Ishiura M. ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells 2003, 8:287-296.
47. Heiland I., Bodenstein C., Hinze T., Weisheit O., Ebenhoeh O., Mittag M., Schuster S. Modeling temperature entrainment of circadian clocks using the Arrhenius equation and a reconstructed model from Chlamydomonas reinhardtii. J. Biol. Phys. 2012, 38:449-464.
48. Hertel S., Brettschneider C., Axmann I.M. Revealing a two-loop transcriptional feedback mechanism in the cyanobacterial circadian clock. PLoS Comput. Biol. 2013, 9:e1002966.
49. Holtzendorff J., Partensky F., Jacquet S., Bruyant F., Marie D., Garczarek L., Mary I., Vaulot D., Hess W.R. Diel expression of cell cycle-related genes in synchronized cultures of Prochlorococcus sp. strain PCC 9511. J. Bacteriol. 2001, 183:915-920.
50. Holtzendorff J., Marie D., Post A.F., Partensky F., Rivlin A., Hess W.R. Synchronized expression of ftsZ in natural Prochlorococcus populations of the Red Sea. Environ. Microbiol. 2002, 4:644-653.
51. Holtzendorff J., Partensky F., Mella D., Lennon J.F., Hess W.R., Garczarek L. Genome streamlining results in loss of robustness of the circadian clock in the marine cyanobacterium Prochlorococcus marinus PCC 9511. J. Biol. Rhythm. 2008, 23:187-199.
52. Huisman J.M., Matthijs H.C.P., Visser P.M. Harmful Cyanobacteria 2005, Springer, Berlin.
53. Ishiura M., Kutsuna S., Aoki S., Iwasaki H., Andersson C.R., Tanabe A., Golden S.S., Johnson C.H., Kondo T. Expression of a gene cluster kaiABC as a circadian feedback process in Cyanobacteria. Science 1998, 281:1519-1523.
54. Ito H., Kageyama H., Mutsuda M., Nakajima M., Oyama T., Kondo T. Autonomous synchronization of the circadian KaiC phosphorylation rhythm. Nat. Struct. Mol. Biol. 2007, 14:1084-1088.
55. Ito H., Mutsuda M., Murayama Y., Tomita J., Hosokawa N., Terauchi K., Sugita C., Sugita M., Kondo T., Iwasaki H. Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14168-14173.
56. Ivleva N.B., Bramlett M.R., Lindahl P.A., Golden S.S. LdpA: a component of the circadian clock senses redox state of the cell. EMBO J. 2005, 24:1202-1210.
57. Ivleva N.B., Gao T., LiWang A.C., Golden S.S. Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17468-17473.
58. Iwasaki H., Taniguchi Y., Ishiura M., Kondo T. Physical interactions among circadian clock proteins KaiA, KaiB and KaiC in Cyanobacteria. EMBO J. 1999, 18:1137-1145.
59. Iwasaki H., Williams S.B., Kitayama Y., Ishiura M., Golden S.S., Kondo T. A KaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in Cyanobacteria 2000, 101:223-233.
60. Iwasaki H., Nishiwaki T., Kitayama Y., Nakajima M., Kondo T. KaiA-stimulated KaiC phosphorylation in circadian timing loops in Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15788-15793.
61. Katayama M., Kondo T., Xiong J., Golden S.S. ldpA encodes an iron-sulfur protein involved in light-dependent modulation of the circadian period in the cyanobacterium Synechococcus elongatus PCC 7942. J. Bacteriol. 2003, 185:1415-1422.
62. Kim Y.-I., Dong G., Carruthers C.W., Golden S.S., LiWang A. The day/night switch in KaiC, a central oscillator component of the circadian clock of Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12825-12830.
63. Kim Y.I., Vinyard D.J., Ananyev G.M., Dismukes G.C., Golden S.S. Oxidized quinones signal onset of darkness directly to the cyanobacterial circadian oscillator. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:17765-17769.
64. Kitayama Y., Iwasaki H., Nishiwaki T., Kondo T. KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J. 2003, 22:2127-2134.
65. Kitayama Y., Nishiwaki T., Terauchi K., Kondo T. Dual KaiC-based oscillations constitute the circadian system of Cyanobacteria. Genes Dev. 2008, 22:1513-1521.
66. Ko C.H., Takahashi J.S. Molecular components of the mammalian circadian clock. Hum. Mol. Genet. 2006, 15(2):R271-R277.
67. Kondo T., Strayer C.A., Kulkarni R.D., Taylor W., Ishiura M., Golden S.S., Johnson C.H. Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:5672-5676.
68. Kutsuna S., Kondo T., Aoki S., Ishiura M. A period-extender gene, pex, that extends the period of the circadian clock in the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 1998, 180:2167-2174.
69. Kutsuna S., Kondo T., Ikegami H., Uzumaki T., Katayama M., Ishiura M. The circadian clock-related gene pex regulates a negative cis element in the kaiA promoter region. J. Bacteriol. 2007, 189:7690-7696.
70. Langlois R.J., Hummer D., LaRoche J. Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Appl. Environ. Microbiol. 2008, 74:1922-1931.
71. Liu H., Nolla H.A., Campbell L. Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat. Microb. Ecol. 1997, 12:39-47.
72. Liu Y., Tsinoremas N.F., Johnson C.H., Lebedeva N.V., Golden S.S., Ishiura M., Kondo T. Circadian orchestration of gene expression in Cyanobacteria. Genes Dev. 1995, 9:1469-1478.
73. Liu Y., Merrow M., Loros J.J., Dunlap J.C. How temperature changes reset a circadian oscillator. Science 1998, 281:825-829.
74. Loza-Correa M., Gomez-Valero L., Buchrieser C. Circadian clock proteins in prokaryotes: hidden rhythms?. Front. Microbiol. 2010, 1:130.
75. Mackey S.R., Choi J.S., Kitayama Y., Iwasaki H., Dong G., Golden S.S. Proteins found in a CikA interaction assay link the circadian clock, metabolism, and cell division in Synechococcus elongatus. J. Bacteriol. 2008, 190:3738-3746.
76. Mackey S.R., Golden S.S., Ditty J.L. The itty-bitty time machine genetics of the cyanobacterial circadian clock. Adv. Genet. 2011, 74:13-53.
77. Mary I., Garczarek L., Tarran G.A., Kolowrat C., Terry M.J., Scanlan D.J., Burkill P.H., Zubkov M.V. Diel rhythmicity in amino acid uptake by Prochlorococcus. Environ. Microbiol. 2008, 10:2124-2131.
78. Millineaux P.M., Gallon J.R., Chaplin A.E. Acetylene reduction (nitrogen fixation) by Cyanobacteria grown under alternating light-dark cycles. FEMS Microbiol. Lett. 1981, 10:245-247.
79. Min H., Guo H., Xiong J. Rhythmic gene expression in a purple photosynthetic bacterium, Rhodobacter sphaeroides. FEBS Lett. 2005, 579:808-812.
80. Mitsui A., Kumazawa S., Takahashi A., Ikemoto H., Cao S., Arai T. Strategy by which nitrogen-fixing unicellular Cyanobacteria grow photoautotrophically. Nature 1986, 323:720-722.
81. Miyoshi F., Nakayama Y., Kaizu K., Iwasaki H., Tomita M. A mathematical model for the Kai-protein-based chemical oscillator and clock gene expression rhythms in Cyanobacteria. J. Biol. Rhythm. 2007, 22:69-80.
82. Moisander P.H., Beinart R.A., Hewson I., White A.E., Johnson K.S., Carlson C.A., Montoya J.P., Zehr J.P. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 2010, 327:1512-1514.
83. Montoya J.P., Holl C.M., Zehr J.P., Hansen A., Villareal T.A., Capone D.G. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 2004, 430:1027-1032.
84. Mori T., Johnson C.H. Circadian programming in Cyanobacteria. Semin. Cell Dev. Biol. 2001, 12:271-278.
85. Mori T., Saveliev S.V., Xu Y., Stafford W.F., Cox M.M., Inman R.B., Johnson C.H. Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:17203-17208.
86. Murayama Y., Mukaiyama A., Imai K., Onoue Y., Tsunoda A., Nohara A., Ishida T., Maeda Y., Terauchi K., Kondo T., Akiyama S. Tracking and visualizing the circadian ticking of the cyanobacterial clock protein KaiC in solution. EMBO J. 2011, 30:68-78.
87. Mutsuda M., Michel K.P., Zhang X., Montgomery B.L., Golden S.S. Biochemical properties of CikA, an unusual phytochrome-like histidine protein kinase that resets the circadian clock in Synechococcus elongatus PCC 7942. J. Biol. Chem. 2003, 278:19102-19110.
88. Nakahira Y., Katayama M., Miyashita H., Kutsuna S., Iwasaki H., Oyama T., Kondo T. Global gene repression by KaiC as a master process of prokaryotic circadian system. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:881-885.
89. Nakajima M., Imai K., Ito H., Nishiwaki T., Murayama Y., Iwasaki H., Oyama T., Kondo T. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 2005, 308:414-415.
90. Nakamura Y., Kaneko T., Sato S., Mimuro M., Miyashita H., Tsuchiya T., Sasamoto S., Watanabe A., Kawashima K., Kishida Y., Kiyokawa C., Kohara M., Matsumoto M., Matsuno A., Nakazaki N., Shimpo S., Takeuchi C., Yamada M., Tabata S. Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res. 2003, 10:137-145.
91. Narikawa R., Kohchi T., Ikeuchi M. Characterization of the photoactive GAF domain of the CikA homolog (SyCikA, Slr1969) of the cyanobacterium Synechocystis sp. PCC 6803. Photochem. Photobiol. Sci. 2008, 7:1253-1259.
92. Ng W.L., Bassler B.L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 2009, 43:197-222.
93. Nishiwaki T., Iwasaki H., Ishiura M., Kondo T. Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:495-499.
94. Nishiwaki T., Satomi Y., Nakajima M., Lee C., Kiyohara R., Kageyama H., Kitayama Y., Temamoto M., Yamaguchi A., Hijikata A., Go M., Iwasaki H., Takao T., Kondo T. Role of KaiC phosphorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13927-13932.
95. Nishiwaki T., Satomi Y., Kitayama Y., Terauchi K., Kiyohara R., Takao T., Kondo T. A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in Cyanobacteria. EMBO J. 2007, 26:4029-4037.
96. Nishiwaki T., Kondo T. Circadian autodephosphorylation of cyanobacterial clock protein KaiC occurs via formation of ATP as intermediate. J. Biol. Chem. 2012, 287:18030-18035.
97. Ottesen E.A., Young C.R., Eppley J.M., Ryan J.P., Chavez F.P., Scholin C.A., DeLong E.F. Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E488-E497.
98. Ouyang Y., Andersson C.R., Kondo T., Golden S.S., Johnson C.H. Resonating circadian clocks enhance fitness in Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8660-8664.
99. Paerl H.W., Otten T.G. Harmful cyanobacterial blooms: causes, consequences, and controls. Microb. Ecol. 2013, 65:995-1010.
100. Partensky F., Blanchot J., Lantoine F., Neveux J., Marie D. Vertical structure of picophytoplankton at different trophic sites of the tropical northeastern Atlantic Ocean. Deep-Sea Res. 1996, 43:1191-1213.
101. Partensky F., Hess W.R., Vaulot D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 1999, 63:106-127.
102. Pattanayek R., Wang J., Mori T., Xu Y., Johnson C.H., Egli M. Visualizing a circadian clock protein: crystal structure of KaiC and functional insights. Mol. Cell 2004, 15:375-388.
103. Pattanayek R., Williams D.R., Pattanayek S., Mori T., Johnson C.H., Stewart P.L., Egli M. Structural model of the circadian clock KaiB-KaiC complex and mechanism for modulation of KaiC phosphorylation. EMBO J. 2008, 27:1767-1778.
104. Pattanayek R., Williams D.R., Rossi G., Weigand S., Mori T., Johnson C.H., Stewart P.L., Egli M. Combined SAXS/EM based models of the S. elongatus post-translational circadian oscillator and its interactions with the output His-kinase SasA. PLoS One 2011, 6:e23697.
105. Pattanayek R., Yadagiri K.K., Ohi M.D., Egli M. Nature of KaiB-KaiC binding in the cyanobacterial circadian oscillator. Cell Cycle 2013, 12:810-817.
106. Pennebaker K., Mackey K.R., Smith R.M., Williams S.B., Zehr J.P. Diel cycling of DNA staining and nifH gene regulation in the unicellular cyanobacterium Crocosphaera watsonii strain WH 8501 (Cyanophyta). Environ. Microbiol. 2010, 12:1001-1010.
107. Qin X., Byrne M., Mori T., Zou P., Williams D.R., McHaourab H., Johnson C.H. Intermolecular associations determine the dynamics of the circadian KaiABC oscillator. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14805-14810.
108. Qin X., Byrne M., Xu Y., Mori T., Johnson C.H. Coupling of a core post-translational pacemaker to a slave transcription/translation feedback loop in a circadian system. PLoS Biol. 2010, 8:e1000394.
109. Reddy K.J., Haskell J.B., Sherman D.M., Sherman L.A. Unicellular, aerobic nitrogen-fixing Cyanobacteria of the genus Cyanothece. J. Bacteriol. 1993, 175:1284-1292.
110. Rippka R., Waterbury J., Cohen-Bazire G. A cyanobacterium which lacks thylakoids. Arch. Microbiol. 1974, 100:419-436.
111. Rippka R., Deruelles J., Waterbury J.B., Herdman M., Stanier R.Y. Generic assignments, strain histories and properties of pure cultures of Cyanobacteria. J. Gen. Microbiol. 1979, 111:1-61.
112. Rust M.J., Markson J.S., Lane W.S., Fisher D.S., O'Shea E.K. Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 2007, 318:809-812.
113. Rust M.J., Golden S.S., O'Shea E.K. Light-driven changes in energy metabolism directly entrain the cyanobacterial circadian oscillator. Science 2011, 331:220-223.
114. Schmitz O., Katayama M., Williams S.B., Kondo T., Golden S.S. CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science 2000, 289:765-768.
115. Shi L., Carmichael W.W., Miller I. Immuno-gold localization of hepatotoxins in cyanobacterial cells. Arch. Microbiol. 1995, 163:7-15.
116. 2-fixing cyanobacterium Crocosphaera watsonii WH 8501. ISME J. 2010, 4:621-632.
117. Shih P.M., Wu D., Latifi A., Axen S.D., Fewer D.P., Talla E., Calteau A., Cai F., Tandeau de Marsac N., Rippka R., Herdman M., Sivonen K., Coursin T., Laurent T., Goodwin L., Nolan M., Davenport K.W., Han C.S., Rubin E.M., Eisen J.A., Woyke T., Gugger M., Kerfeld C.A. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1053-1058.
118. Simons M.J. The evolution of the cyanobacterial posttranslational clock from a primitive "phoscillator". J. Biol. Rhythm. 2009, 24:175-182.
119. Smith R.M., Williams S.B. Circadian rhythms in gene transcription imparted by chromosome compaction in the cyanobacterium Synechococcus elongatus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8564-8569.
120. Stal L., Krumbein W. Nitrogenase activity in the non-heterocystous cyanobacterium Oscillatoria sp. grown under alternating light-dark cycles. Arch. Microbiol. 1985, 143:67-71.
121. Stal L.J., Krumbein W.E. Temporal separation of nitrogen fixation and photosynthesis in the filamentous, non-heterocystous cyanobacterium Oscillatoria sp. Arch. Microbiol. 1987, 149:76-80.
122. Stöckel J., Welsh E.A., Liberton M., Kunnvakkam R., Aurora R., Pakrasi H.B. Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6156-6161.
123. Stöckel J., Jacobs J.M., Elvitigala T.R., Liberton M., Welsh E.A., Polpitiya A.D., Gritsenko M.A., Nicora C.D., Koppenaal D.W., Smith R.D., Pakrasi H.B. Diurnal rhythms result in significant changes in the cellular protein complement in the cyanobacterium Cyanothece 51142. PLoS One 2011, 6:e16680.
124. Straub C., Quillardet P., Vergalli J., de Marsac N.T., Humbert J.F. A day in the life of Microcystis aeruginosa strain PCC 7806 as revealed by a transcriptomic analysis. PLoS One 2011, 6:e16208.
125. Sweeney B.M., Borgese M.B. A circadian rhythm in cell division in a prokaryote, the cyanobacterium Synechococcus WH7803. J. Phycol. 1989, 25:183-186.
126. Takai N., Nakajima M., Oyama T., Kito R., Sugita C., Sugita M., Kondo T., Iwasaki H. A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:12109-12114.
127. Taniguchi Y., Katayama M., Ito R., Takai N., Kondo T., Oyama T. labA: a novel gene required for negative feedback regulation of the cyanobacterial circadian clock protein KaiC. Genes Dev. 2007, 21:60-70.
128. Taniguchi Y., Takai N., Katayama M., Kondo T., Oyama T. Three major output pathways from the KaiABC-based oscillator cooperate to generate robust circadian kaiBC expression in Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3263-3268.
129. Teng S.W., Mukherji S., Moffitt J.R., de Buyl S., O'Shea E.K. Robust circadian oscillations in growing Cyanobacteria require transcriptional feedback. Science 2013, 340:737-740.
130. Terauchi K., Kitayama Y., Nishiwaki T., Miwa K., Murayama Y., Oyama T., Kondo T. ATPase activity of KaiC determines the basic timing for circadian clock of Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16377-16381.
131. Thompson A.W., Foster R.A., Krupke A., Carter B.J., Musat N., Vaulot D., Kuypers M.M., Zehr J.P. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 2012, 337:1546-1550.
132. Toepel J., Welsh E., Summerfield T.C., Pakrasi H.B., Sherman L.A. Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. J. Bacteriol. 2008, 190:3904-3913.
133. Tomita J., Nakajima M., Kondo T., Iwasaki H. No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 2005, 307:251-254.
134. Tripp H.J., Bench S.R., Turk K.A., Foster R.A., Desany B.A., Niazi F., Affourtit J.P., Zehr J.P. Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 2010, 464:90-94.
135. Tseng R., Chang Y.G., Bravo I., Latham R., Chaudhary A., Kuo N.W., Liwang A. Cooperative KaiA-KaiB-KaiC Interactions Affect KaiB/SasA Competition in the Circadian Clock of Cyanobacteria. J. Mol. Biol. 2014, 426:389-402.
136. Tu B.P., McKnight S.L. Metabolic cycles as an underlying basis of biological oscillations. Nat. Rev. Mol. Cell Biol. 2006, 7:696-701.
137. Vakonakis I., LiWang A.C. Structure of the C-terminal domain of the clock protein KaiA in complex with a KaiC-derived peptide: implications for KaiC regulation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10925-10930.
138. van Gremberghe I., Van Wichelen J., Van der Gucht K., Vanormelingen P., D'Hondt S., Boutte C., Wilmotte A., Vyverman W. Covariation between zooplankton community composition and cyanobacterial community dynamics in Lake Blaarmeersen (Belgium). FEMS Microbiol. Ecol. 2008, 63:222-237.
139. van Zon J.S., Lubensky D.K., Altena P.R., ten Wolde P.R. An allosteric model of circadian KaiC phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:7420-7425.
140. Vaulot D., Marie D., Olson R.J., Chisholm S.W. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific Ocean. Science 1995, 268:1480-1482.
141. Vaulot D., Marie D. Diel variability of photosynthetic picoplankton in the equatorial Pacific. J. Geophys. Res. 1999, 104:3297-3310.
142. Vijayan V., Zuzow R., O'Shea E.K. Oscillations in supercoiling drive circadian gene expression in Cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:22564-22568.
143. Villarreal S.A., Pattanayek R., Williams D.R., Mori T., Qin X., Johnson C.H., Egli M., Stewart P.L. CryoEM and molecular dynamics of the circadian KaiB-KaiC complex indicates KaiB monomers interact with KaiC and block ATP binding clefts. J. Mol. Biol. 2013, 425:3311-3324.
144. Vogel J., Axmann I.M., Herzel H., Hess W.R. Experimental and computational analysis of transcriptional start sites in the cyanobacterium Prochlorococcus MED4. Nucleic Acids Res. 2003, 31:2890-2899.
145. Voß B., Bolhuis H., Fewer D.P., Kopf M., Moke F., Haas F., El-Shehawy R., Hayes P., Bergman B., Sivonen K., Dittmann E., Scanlan D.J., Hagemann M., Stal L.J., Hess W.R. Insights into the physiology and ecology of the brackish-water-adapted Cyanobacterium Nodularia spumigena CCY9414 based on a genome-transcriptome analysis. PLoS One 2013, 8:e60224.
146. Waldbauer J.R., Rodrigue S., Coleman M.L., Chisholm S.W. Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle. PLoS One 2012, 7:e43432.
147. Walker J.E., Saraste M., Runswick M.J., Gay N.J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982, 1:945-951.
148. Walsby A.E. Gas vesicles. Microbiol. Rev. 1994, 58:94-144.
149. Whitton B.A., Potts M. Introduction to Cyanobacteria. The Ecology of Cyanobacteria 2000, 1-11. Klewer Academic, Amsterdam. B.A. Whitton, M. Potts (Eds.).
150. Wiegard A., Dörrich A.K., Deinzer H.T., Beck C., Wilde A., Holtzendorff J., Axmann I.M. Biochemical analysis of three putative KaiC clock proteins from Synechocystis sp. PCC 6803 suggests their functional divergence. Microbiology 2013, 159:948-958.
151. Williams S.B., Vakonakis I., Golden S.S., LiWang A.C. Structure and function from the circadian clock protein KaiA of Synechococcus elongatus: a potential clock input mechanism. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15357-15362.
152. Williams S.B. A circadian timing mechanism in the Cyanobacteria. Adv. Microb. Physiol. 2007, 52:229-296.
153. Williams S.B. Speculation and hoopla: is diversity expected in cyanobacterial circadian timing systems?. Bacterial Circadian Programs 2009, 19-38. Springer. J.L. Ditty, S.R. Mackey, C.H. Johnson (Eds.).
154. Woelfle M.A., Ouyang Y., Phanvijhitsiri K., Johnson C.H. The adaptive value of circadian clocks: an experimental assessment in Cyanobacteria. Curr. Biol. 2004, 14:1481-1486.
155. Woelfle M.A., Xu Y., Qin X., Johnson C.H. Circadian rhythms of superhelical status of DNA in cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18819-18824.
156. Wood T.L., Bridwell-Rabb J., Kim Y.I., Gao T., Chang Y.G., LiWang A., Barondeau D.P., Golden S.S. The KaiA protein of the cyanobacterial circadian oscillator is modulated by a redox-active cofactor. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5804-5809.
157. Xu Y., Mori T., Johnson C.H. Cyanobacterial circadian clockwork: roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J. 2003, 22:2117-2126.
158. Xu Y., Mori T., Pattanayek R., Pattanayek S., Egli M., Johnson C.H. Identification of key phosphorylation sites in the circadian clock protein KaiC by crystallographic and mutagenetic analyses. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13933-13938.
159. Xu Y., Mori T., Qin X., Yan H., Egli M., Johnson C.H. Intramolecular regulation of phosphorylation status of the circadian clock protein KaiC. PLoS One 2009, 4:e7509.
160. Xu Y., Ma P., Shah P., Rokas A., Liu Y., Johnson C.H. Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 2013, 495:116-120.
161. Yang Q., Pando B.F., Dong G., Golden S.S., van Oudenaarden A. Circadian gating of the cell cycle revealed in single cyanobacterial cells. Science 2010, 327:1522-1526.
162. 2 in the subtropical North Pacific Ocean. Nature 2001, 412:635-638.
163. 2-fixing Cyanobacteria lack oxygenic photosystem II. Science 2008, 322:1110-1112.
164. Zhang X., Dong G., Golden S.S. The pseudo-receiver domain of CikA regulates the cyanobacterial circadian input pathway. Mol. Microbiol. 2006, 60:658-668.
165. Zinser E.R., Lindell D., Johnson Z.I., Futschik M.E., Steglich C., Coleman M.L., Wright M.A., Rector T., Steen R., McNulty N., Thompson L.R., Chisholm S.W. Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, Prochlorococcus. PLoS One 2009, 4:e5135.
166. Zwicker D., Lubensky D.K., Ten Wolde P.R. Robust circadian clocks from coupled protein-modification and transcription-translation cycles. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:22540-22545.